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in foods on children’s preference and intake

Sofia Bouhlal

To cite this version:

Sofia Bouhlal. Consequence of salt, sugar and fat content modifications in foods on children’s prefer- ence and intake. Food and Nutrition. Université de Bourgogne, 2011. English. �NNT : 2011DIJOS110�.

�tel-01684238�

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UNIVERSITY OF BURGUNDY

Ecole Doctorale Environnement, Santé, STIC n°490

PhD THESIS To obtain the degree of Doctor of the University of Burgundy

Discipline: Food Sciences

Presented by

Sofia BOUHLAL

Consequence of salt, sugar and fat content modifications in foods on children’s preference and intake

PhD defence scheduled on December 21st, 2011, in presence of a jury composed of:

Pr. Marion Hetherington University of Leeds, United Kingdom Reviewer Dr. Remco Havermans Maastricht University, The Netherlands Reviewer Pr. Catherine Dacremont University of Burgundy, France Examiner Dr. Sandrine Péneau UMR UREN, U557, Bobigny, France Examiner Dr. Sylvie Issanchou UMR CSGA, INRA, Dijon, France Supervisor Dr. Sophie Nicklaus UMR CSGA, INRA, Dijon, France Co-supervisor

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UNIVERSITE DE BOURGOGNE

Ecole Doctorale Environnement, Santé, STIC n°490

THÈSE DE DOCTORAT

Pour obtenir le grade de Docteur de l’Université de Bourgogne

Discipline : Sciences de l’Alimentation

Présentée par

Sofia BOUHLAL

Conséquences des variations de teneur en sel, sucre et matière grasse sur les préférences et les consommations

alimentaires des enfants

Soutenance de thèse prévue le 21 décembre 2011, devant un jury composé de:

Pr. Marion Hetherington Université de Leeds, Royaume Uni Rapporteur Dr. Remco Havermans Université de Maastricht, Pays-Bas Rapporteur Pr. Catherine Dacremont Université de Bourgogne, France Examinateur Dr. Sandrine Péneau UMR UREN, U557, Bobigny, France Examinateur Dr. Sylvie Issanchou UMR CSGA, INRA, Dijon, France Directrice de thèse Dr. Sophie Nicklaus UMR CSGA, INRA, Dijon, France Co-directrice de thèse

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Comme toute bonne recette, la préparation d’une thèse est un processus très délicat. La parfaire requiert beaucoup d’affection, d’attention, de rigueur et de patience. A l’image de l’importance que peut avoir la qualité et la nature des ingrédients qui composent une recette, la nature et la valeur des expériences vécues pendant une thèse contribuent à la rendre unique. Ces expériences sont souvent le fruit de rencontres avec des personnes exceptionnelles. Tout comme le secret d’une recette réside dans la liste des ingrédients qui y sont incorporés, qu’ils soient ajoutés au début, pendant ou à la fin de la recette, plusieurs acteurs entrent en scène à différents moment de cette aventure. Cette liste de personnes qui jouent un rôle majeur dans la réussite d’une expérience de thèse est différent d’un thésard à l’autre; voici la mienne…

Tout d’abord, je vais remercie les personnes qui ont participés à la dernière -mais néanmoins peu négligeable- étape de cette thèse: with all my affection and respect, I would like to thank Marion Hetherington and Remco Havermans who kindly accepted to discuss and judge my work. J’aimerais également remercier Catherine Dacremont et Sandrine Péneau d’avoir accepté de faire partie de mon jury de thèse, ainsi que Vincent Boggio, Natalie Rigal et Kees De Graaf pour m’avoir conseillés et guidés dans ce travail. Merci également au Conseil Régional de Bourgogne pour avoir financé ce travail.

Ma thèse n’aurait jamais été l’agréable expérience qu’elle fut sans Sophie Nicklaus et Sylvie Issanchou. Merci pour votre disponibilité, votre patience et pour l’inspiration que vous avez été pour moi et pour mon travail. Merci de m’avoir aidé à murir mes réflexions scientifiques. Grâce à votre ouverture d’esprit, votre clairvoyance et votre grande rigueur scientifique, vous avez grandement contribué à façonner le chercheur en moi. Je n’oublierais jamais nos discussions passionnées autours de théories un peu capillo-tractées, et les nombreux fous rires pendant les différents ‘points’ de corrections en stéréo. MERCI!

Une mention très spéciale pour Claire Chabanet, merci de m’avoir si patiemment et efficacement guidée à travers les ruelles sombres de statisticville. Grâce a toi les statistiques n’auront plus de mystères pour moi (ou presque!!).

Ce travail n’aurait jamais vu le jour sans l’implication et l’enthousiasme des membres du service de la petite enfance de la Ville de Dijon: Mmes Tenembaume, Barney et Kreitter.

Sans oublier les chefs, équipes et directrices des crèches Gaffarel, Montchapet, Voltaire, Gresille, Fontaine d’Ouche, Roosevelt et Junot. Je n’oublie pas Mme Catherine Laurent et toute l’équipe de l’école Saint Dominique. Merci à tous de m’avoir fait confiance et de nous avoir accueillis à bras ouverts et aidés lors des expériences. Un très très grand merci aux parents et aux enfants, j’espère vous avoir régalés avoir tous ces bons mets.

Je n’oublie pas de remercier chaleureusement les ‘brigades en cuisine’ qui ont aidées aux différentes étapes des études. A commencer par remercier Valérie et Emilie, sans qui les

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conduite des profils sensoriels.

Merci à toutes les personnes croisées aux détours des couloirs pour votre soutien, votre sourire et pour avoir contribué à faire de cette thèse une aventure humaine extraordinaire.

Un clin d’œil aux habitants du 050 pour leur bonne humeur et surtout à Thierry pour ses conseils avisés et pour les discussions passionnantes (pas toujours qu’en sciences d’ailleurs!).

Je n’oublie pas de remercier les ‘Castors’ [a.k.a. Chloé, Chacha, Juju, Pierre, Eric et mon Charly], pour les merveilleux moments qu’on a partagés. Je me rappellerais avec le sourire et beaucoup de nostalgie de nos soirées ‘restaurant gastronomique’ suivi du visionnage de films historiques ! Bon courage à vous tous …

Je ne peux pas finir ma liste sans remercier ma famille. En commençant par mes

« parents » d’adoption Nicole et Jean Louvet. Je vous remercie du fond du cœur d’avoir enrichi mon expérience Dijonnaise et de m’avoir fait découvrir la Bourgogne, ses bons petits plats et ses châteaux.

Un énorme merci a ma sœur et a mes parents pour avoir toujours cru en moi, en mes décisions et avoir validé mes choix sans poser de question. En somme merci de m’avoir permis de vivre ma vie pleinement, je vous adore !

And last but not least, je remercie ma meilleure moitié et mon meilleur ami, Tony, d’avoir été là tout au long de ces années intenses. Merci de m’avoir soutenu malgré la distance, de m’avoir parlé et réconforté quand j’en avais besoin et de m’avoir écouté et conseillé quand j’en avais besoin.

Merci à tous de m’avoir supporté et supporté pendant ces belles années.

Avec une Dream-Team comme celle-ci, l’expérience de thèse ne pouvait être qu’une réussite.

Don’t you think ?

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Table of contents

Table of contents ___________________________________________________________ i List of Abbreviations _______________________________________________________ iv List of tables _______________________________________________________________ v List of figures _____________________________________________________________ vi General introduction ________________________________________________________ 9 Chapter 1. Literature review _________________________________________________ 17 Part 1. Relevance of research on salt, sugar and fat ______________________________ 18 1.1 Functions of these ingredients ________________________________________________ 18

1.1.1. The technological and the hygienic roles of salt, sugar and fat ____________________________ 18 1.1.2. The organoleptic functions of salt, sugar and fat _______________________________________ 19 1.1.3. The nutritional and physiological functions of salt, sugar and fat __________________________ 21

1.2. Public health concerns related to salt, sugar and fat intake ________________________ 24 1.2.1. Diet-related health problems in relation to salt, sugar and fat intake ________________________ 24

1.2.1.1. Salt ______________________________________________________________________ 24 1.2.1.2. Sugar ____________________________________________________________________ 26 1.2.1.3. Fat ______________________________________________________________________ 27

1.2.2. Body weight and nutrient intakes __________________________________________________ 28 1.2.2.1. Definition of overweight and obesity ____________________________________________ 28 1.2.2.2. Cut-offs and prevalence of overweight and obesity in adults _________________________ 29 1.2.2.3. Cut-offs and prevalence of overweight and obesity in children ________________________ 29 1.2.2.4. Dietary factors involved in the etiology of overweight and obesity ____________________ 33

1.3. Public health recommendations and actions ____________________________________ 37 1.3.1. General recommendations ________________________________________________________ 37 1.3.2. Recommendations targeting the food industry and catering ______________________________ 41 1.3.3. Recommendations targeting the consumers___________________________________________ 44

1.4. Intake data: national and international surveys _________________________________ 46 1.4.1. Salt intake ____________________________________________________________________ 46 1.4.2. Sugar and fat intake _____________________________________________________________ 47 1.4.3. Exposure to salt, sugar and fat, and their intake during early feeding experiences _____________ 48

Part 2. Development of taste perceptions _______________________________________ 52 2.1. Taste: what are we talking about? ____________________________________________ 52 2.2. How do we perceive tastes? __________________________________________________ 53

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2.2.1. From the reception to the perception of the gustatory information _________________________ 53 2.2.2. The particular case of fatty taste ___________________________________________________ 59

2.3. Early development of the human gustatory system ______________________________ 62 2.3.1 Anatomical changes _____________________________________________________________ 62 2.3.2. Methodological investigations _____________________________________________________ 63

2.4. Sensory interactions involving taste ___________________________________________ 66 2.4.1. Interactions involving saltiness ____________________________________________________ 67 2.4.2. Interactions involving sweetness ___________________________________________________ 69

Part 3. Tastes: From detection to behavior ______________________________________ 70 3.1. Sensory testing with newborns, infants, toddlers and older children ________________ 70

3.2. Impact of salt, sugar and fat content modifications in foods on hedonic responses _____ 74 3.2.1. Effect of salt on hedonics ________________________________________________________ 75 3.1.2. Effect of sugar on hedonics _______________________________________________________ 79 3.1.3. Effect of fat on hedonics _________________________________________________________ 82 3.1.4. Is there a link between weight status and preference for salt, sugar or fat in foods? ____________ 85

3.2. Impact of salt, sugar and fat on food intake ____________________________________ 88 3.2.1. Food intake: definitions and background _____________________________________________ 88 3.2.2. Effect of salt on intake ___________________________________________________________ 90 3.2.3. Effect of sugar on intake _________________________________________________________ 91 3.2.4. Effect of fat on intake ___________________________________________________________ 92 3.2.5. Is there a link between weight status and intake of salt, sugar or fat in foods? ________________ 93 3.3. Link between preference and intake __________________________________________ 94 Part 4. Exposure and learning mechanisms involved in the acquisition of food preferences _________________________________________________________________________ 96

4.1. Mere exposure mechanism __________________________________________________ 96 4.2. Flavor-flavor learning mechanism ___________________________________________ 100 4.3. Flavor-nutrient learning ___________________________________________________ 105

4.4. Comparison between mechanisms ___________________________________________ 108 4.4.1. What influences the efficiency of mechanisms _______________________________________ 108 4.4.2. Can learning effects be separated as ME, FFL and FNL? _______________________________ 109

Part 5. Thesis outline and research questions ___________________________________ 111 Chapter 2. The impact of salt, sugar and fat on toddlers’ food intake ________________ 115 Chapter 3. Salt content: effect on preferences and consequences on intake in children _ 125 Chapter 4. ‘Just a pinch of salt’: conditioning vegetable acceptance in toddlers with salt or spice ____________________________________________________________________ 145

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Participants and methods ___________________________________________________ 150 Results __________________________________________________________________ 158 Discussion _______________________________________________________________ 164 Conclusions _____________________________________________________________ 168 Chapter 5. The different impact of fat content on toddlers’ and adults’ food intake ____ 173 Chapter 6. Summary of results and general discussion ___________________________ 195 1. Main findings ______________________________________________________________ 196

1.1. Salt impact on toddlers’ and children’s food intake and preferences ________________________ 196 1.2. Sugar impact on toddlers’ food intake _______________________________________________ 201 1.3. Fat impact on toddlers’ and adults’ food intake and preferences ___________________________ 202 2. Methodological considerations and experimental approach ________________________ 204 3. General discussion__________________________________________________________ 212 4. Implications _______________________________________________________________ 214 5. Perspectives _______________________________________________________________ 216 6. Conclusions _______________________________________________________________ 219

References _______________________________________________________________ 220 Appendices ______________________________________________________________ 220 Abstract

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List of Abbreviations

AFSSA Agence Française de Sécurité Sanitaire des Aliments - French Food Safety Agency

ANC/RDA Apports Nutritionnels Conseillés – Recommended Dietary Allowance

ANSES1 Agence nationale de sécurité sanitaire de l'alimentation, de l'environnement et du travail - French Agency for Food, Environmental and Occupational Health and Safety

BP Blood Pressure

COMA Committee on Medical Aspects of Foods (USA) CS Conditioned Stimulus

CVD Cardiovascular diseases

CWC Creamy White Cheese

ED Energy density

EFA Essential Fatty Acids

EI Energy intake

FFL Flavor-Flavor Learning FNL Flavor-Nutrient Learning

FSAI Food Safety Authority of Ireland

GB Green bean

IHF Irish Heart Foundation

INCA Enquête Individuelle et nationale de Consommation Alimentaire – National Individual survey of eating habits (France)

Inserm Institut national de la santé et de la recherche médicale – National Institute for Health and Medical Research (France)

IOM Institute Of Medicine (USA)

ME Mere Exposure

MUFA Monounsaturated Fatty Acids

PNNS National Nutrition and Health Program - Programme National Nutrition Santé- (France)

PUFA Polyunsaturated Fatty Acids RSM Response Surface Method

SACN Scientific Advisory Committee on Nutrition (UK) SFA Saturated Fatty Acids

US Unconditioned Stimulus WHO World Health Organization

1 The ANSES was founded on the 1st July 2010 following the merger of two French health agencies: the French Food Safety Agency (AFSSA) and the French Agency for Environmental and Occupational Health Safety (AFSSET).

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List of tables

Table 1. French dietary guidelines (PNNS). ... 11

Table 2. Evolution of the prevalence of overweight and obesity in French children from 1998 to 2007. ... 32

Table 3. Comparison of recommendations regarding total fat dietary intake (% of energy intake), for children 0 to 3 years. ... 40

Table 4. French population references intakes or recommended dietary allowances (ANCs) for fats. ... 41

Table 5. The PNNS1 (2001-06) actions targeting the consumer... 45

Table 6. Average adults’ salt intake by country. ... 46

Table 7. Compliance of the French population with the nutritional recommendations. ... 48

Table 8. Composition of human Caucasian women’s, bovine and infant formula milk.. ... 49

Table 9. Average detection thresholds of fatty acids in humans. ... 60

Table 10. Cognitive skills and advised sensory evaluation methods with children 0 to 12 years. Adapted from ASTM’s Committee 18 on Sensory Evaluation: ASTM, 2003. ... 73

Table 11. Example of studies investigating flavor-flavor learning in children and in adults. 104 Table 12. Comparison between ME, FFL and FNL. ... 110

Table 13. Comparison between the French population's socioeconomic status (SES) and that of parents of toddlers participating in the study from chapter 6. ... 210

Table 14. Summary of the number of toddlers and children involved in the PhD work. ... 211

Table 15. Difference of energy density (kcal) between target food variants, and its effect on intake. ... 213

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List of figures

Figure 1. French Body Mass Index curve. ... 31

Figure 2. Obesity development and its early origins. . ... 34

Figure 3. Monthly distribution of French infants’ relative exposure to basic tastes. ... 51

Figure 4. Taste-receptor cells, buds and papillae. ... 54

Figure 5. Cell to cell communication in the taste buds’. ... 55

Figure 6. Primary processes of taste cells and transduction models. ... 56

Figure 7. Schematic diagram of the brain pathways, responsible among other perceptions, of taste perception.. ... 58

Figure 8. Representation of the global taste reactivity of infants of three age groups: 3, 6 and 12 month-old. ... 63

Figure 9. The evolution of ingestion ratio (IR) of a fat solution at the ages of 3, 6, 12 and 20 months. ... 65

Figure 10. Idealized forms of some possible types of hedonic responses according to the concentration of a stimulus. ... 74

Figure 11. The preponderance of «pleasantness » or « unpleasant” judgments in relation to the stimulus concentrations, for means of groups of several subjects. ... 75

Figure 12. Evolution of 3, 6 and 12 month-old infants' acceptance to salty taste in solution. 76 Figure 13. Five to seven month-old infants' reaction and acceptance of new foods at the beginning of complementary feeding. ... 77

Figure 14. Evolution of 3, 6 and 12 month-old infants' acceptance to sweet taste in solution ... 80

Figure 15. Combined ratings of pleasantness and perceived fat content responses to 8 foods. ... 84

Figure 16. Three dimensional hedonic response surface (top panel) and isopreference contours (bottom panel) of hedonic preference ratings for dairy products with differing sucrose (0, 5, 10 or 20%) and fat (0.1, 3.5, 11.7, 37.6 and 52.6%) contents. ... 87

Figure 17. The Satiety cascade, revised. ... 89

Figure 18. Mean consumption of increasingly sweetened water and orangeades, by subjects 8-10, 14-16 and 20-25 years of age. ... 91

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Figure 19. The relationship between the position in preference order of sandwiches with different spreads, and their intake by 3-4 year toddlers. . ... 95 Figure 20. Flavor experiences throughout childhood. ... 97 Figure 21. Effect of mere exposure on the intake of an initially disliked and an initially liked vegetable. ... 100 Figure 22. Mean ranking scores of 4-6 year-olds for vegetables, before and after a flavor- flavor learning, with sweet taste as the US. ... 102 Figure 23. Effectiveness of flavor-flavor learning on liking of 2-5 year-old initial likers or dislikers of a grapefruit-juice. ... 103 Figure 24. Effect of hunger state on flavor-nutrient learning or mere exposure on 3-4 year- olds' preference for a high-energy (HE) or a low-energy (LE) paired flavors. ... 106 Figure 25. A 'failed' flavor-nutrient learning experiment inducing vegetable liking in 7-8 year- olds.. ... 108 Figure 26. Annual increase in height for age, sex, for French children. ... 204

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General introduction

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General introduction

“To improve your health, the quality of your life and your lifespan, cut down on your consumption of salt, sugar and fat”. This general idea is relayed by several public health authorities around the world.

Attractive foods are generally those containing fat, sugar and salt or their combination (Drewnowski, 1995). Salt (NaCl), sugar (sucrose) and fat (dietary fat) are key ingredients with a great contribution to food structure, food taste and food intake and consequently to body composition. They are believed to be related to many health problems, so called ‘diet- related diseases’; with the most known ones being overweight and obesity, leading in particular to cardiovascular diseases (CVD). This association led the governments to give guidelines and policies in order to lower energy density intake and improve the global health (WHO, 2003). These advices are in form of 1) qualitative targets, as to reducing the levels of salty, sweet and fatty foods’ intake, and 2) quantitative targets (in terms of percent of energy or numbers of grams per day), by advising a reduction of salt, sugar and fat quantities in food preparations for the general population and for children in particular. In France, to reach these objectives, the National Nutrition and Health Program (“Programme National Nutrition Santé” or “PNNS”; Table 1) was set in 2001 and is still on-going (Hercberg, Chat- Yung & Chauliac, 2008).

Few studies to date have evaluated the impact of the advised reductions on food preferences and intake, in particular in young children. Scientific evidences highlighted the influence of salt, sugar and fat in young children’s eating behavior (Drewnowski, 1997a), and the importance of early childhood in the development, establishment and long standing of later food habits (Nicklaus, Boggio, Chabanet & Issanchou, 2005a). Therefore, studying the impact of recommendations such as decreasing salt, sugar and fat content in foods on children’s food intake, seems necessary in order to understand better their role as primary determinants of food preferences and intake.

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Table 1.French dietary guidelines (PNNS). Source: Hercberg et al., 2008.

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During the present thesis, we aimed at understanding the role of salt, sugar and fat content on food preference, liking and intake. The goal was to experiment the impact of subtle -but well perceived- modifications of these ingredients on commonly eaten foods 1) among children in natural settings such as nursery or school canteens 2) and to describe their sensory properties by adults.

In the first chapter of the present manuscript, we will present a literature review explaining the basis of our interest on salt, sugar and fat in early childhood. This five-section chapter will start with a section including a brief overview of the various roles of these three ingredients as technological/hygienic, sensory and physiological contributors; followed by a description of the role they might play on the prevalence of diet-related diseases and especially on overweight and obesity; and by a presentation of the governmental policies and recommendations taken, on the light of intake data collected via national surveys. In the second section, we will present an outline of the development of the perception of these ingredients from birth to early adulthood. A third section will deal with the impact of these ingredients on hedonic responses and food intake. The fourth section of the first chapter will discuss and present the contribution of these ingredients to learning to prefer and consume foods by children. This literature review will be concluded by the research questions raised during the thesis work and its objectives. Chapters 2 to 5 will present the experimental works conducted during the thesis, and will be followed by a last chapter presenting a summary and a general discussion of the thesis findings, and ruled off by suggestions for future researches.

Before starting, few terms that will be used in the present manuscript should be defined:

- Salt refers to sodium chloride (NaCl or table salt). Many kinds of other salts exist (e.g. KCl, LiCl, L-arginine, Na-acetate…). We used NaCl as it represents the major salt used while preparing foods and the one pointed out by public health authorities and nutritional recommendations.

- Sugars, referring to the chemical definition, are the compounds resulting from the combination of carbon, hydrogen and oxygen atoms. They are classified as mono-, di- or oligosaccharides, and they provide 4 kcal / g (15.7 kJ / g). In the present work, we focused on sucrose or table sugar, a disaccharide composed of a combination of glucose and fructose, and we will talk about ‘sugar’.

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- Fat. In most of the text, fat will refer to dietary fat in general and not to a specific fat quality, unless specified. Most dietary fats found in foods are in the form of triglycerides (a glycerol and three attached fatty acids). Fatty acids are classified into three groups:

saturated (SFA; abundant for example in butter), monounsaturated (MUFA; abundant for example in olive oil) and polyunsaturated (PUFA; abundant for example in sunflower oil).

Dietary fats provide the body with 9 kcal / g (35.3 kJ / g), representing its most concentrated source of energy. During this work, fat variations concerned the saturated fatty acid form;

we used butter and dairy products (mainly composed of SFA) where the percent of fat varied.

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List of publication and presentation arising from thesis

Publications:

Bouhlal S., Issanchou S. & Nicklaus S. (2011). The impact of salt, fat and sugar levels on toddler food intake. British Journal of Nutrition, 105, pp 645-653 doi:

10.1017/S0007114510003752.

 Nicklaus S., Bouhlal S., et al. (2010). Development of fat preferences in children (Développement des préférences pour les lipides chez l'enfant). Innovations Agronomiques 10: 115-124.

Bouhlal S., Chabanet C., Issanchou S., & Nicklaus S. (Submitted). Salt content: effect on preferences and consequences on intake in children. Journal of the American Dietetic Association.

Bouhlal S., Issanchou S., & Nicklaus S. (Submitted). The different impact of fat content on toddlers’ and adults’ food intake. Food Quality and Preference.

Bouhlal S., Issanchou S., & Nicklaus S. (In preparation). ‘Just a pinch of salt’: conditioning vegetable acceptance in toddlers with salt or spice.

Oral presentations:

Bouhlal S., Issanchou S. & Nicklaus S. (2011). “Mysterious fat. The different impact of fat on toddlers’ and adults’ food intake” 19th meeting of the Society for the Study of Ingestive Behavior, 12-16 July, 2011, Clearwater, Florida, USA.

Bouhlal S. (2010). Impact de la teneur en sel sur les consommations et les préférences alimentaires d’enfants de 8 à 11 ans. Young Investigators’ Forum. University of Franche- Comté, Besançon, France.

Bouhlal S. (2010). Le sel dans l'alimentation du jeune enfant : effet sur les préférences, conséquences sur les consommations. Internal PhD candidate workshop, Centre des Science du Goût et de l'Alimentation, Dijon, France.

Bouhlal S., Chabanet, C., Issanchou S. & Nicklaus S. (2010). Le sel dans l'alimentation du jeune enfant: effet sur les préférences, conséquences sur les consommations. 8èmes Journées Francophones de Nutrition. Lille, France.

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Poster presentations:

Bouhlal S., Bernard C., Issanchou S. & Nicklaus S. (2011). “Sugar content impacts food intake in toddlers, but could be reduced”. 19th meeting of the Society for the Study of Ingestive Behavior, 12-16 July, 2011, Clearwater, Florida, USA.

Bouhlal S., Issanchou S. & Nicklaus S. (2010). The impact of salt level on children's food intake and preferences. Conference on Feeding and Eating in Infancy and Early Childhood.

The Institute of Child Health, London, UK.

Bouhlal S., Issanchou S. et Nicklaus S. (2009). Does toddlers' food intake differ according to variations in fat, salt or sugar in foods? Young Investigators’ Forum (Forum des jeunes chercheurs). Dijon, France. Award for the best poster.

Bouhlal S., Issanchou S. & Nicklaus S. (2009). How does fat content of a snack food impact toddlers’ and adults’ intake? 8th Pangborn Sensory Science Symposium, Florence, Italy.

Abstracts published in scientific journals:

Bouhlal S., Issanchou S. & Nicklaus S. (2011). “Mysterious fat. The different impact of fat on toddlers’ and adults’ food intake” Appetite 57(1): S6-S7.

doi:10.1016/j.appet.2011.05.131.

Bouhlal S., Bernard C., Issanchou S., Nicklaus S. (2011). “Sugar content impacts food intake in toddlers, but could be reduced” Appetite 57 (1): S7.

doi:10.1016/j.appet.2011.05.132.

Bouhlal S., Issanchou S. et Nicklaus S. (2008). "Does toddlers' food intake differ according to variations in fat, salt or sugar in foods?” Appetite 51 (2): 355.

doi:10.1016/j.appet.2008.04.044

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Chapter 1. Literature review

Part 1. Relevance of research on salt, sugar and fat Part 2. Development of taste perceptions

Part 3. Tastes: from detection to behaviour

Part 4. Learning mechanisms involved in eating behaviour

Part 5. Research questions and thesis outline

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Part 1. Relevance of research on salt, sugar and fat

1.1 Functions of these ingredients

1.1.1. The technological and the hygienic roles of salt, sugar and fat

The role of salt. During the manufacturing process of a large number of products, manufacturers add salt for hygienic and/or technical reasons. Since prehistoric times, salt has always been used to preserve foods for extended periods, due to its bacteriostatic function; it lowers water activity below the threshold needed for bacterial growth; e.g.

Pseudomonas, Escherichia, Bacillus … (Hergarty, 1995 in Lee, 2011). In the case of meat products for example, salt appears to be an important technical ingredient, as one of its roles is to give the typical coloring of meat (Durack, Alonso-Gomez & Wilkinson, 2008). In the bread-making sector salt is added as it contributes to enhance the bread volume, it improves its appearance and it also promotes a good color crust (AFSSA, 2002). In the cheese sector salt is added during the ‘maturation’, a key stage in the manufacturing process that insures a balance of moisture and solids. Adding salt to cheese insures its adequate evolution during ripening, the development of the identifying characteristics of the finished product and it also insures safety during aging (AFSSA, 2002).

The role of sugars. Depending on their type, and beyond their perceived sweet taste, sugars influence safety or quality in many different ways. They increase the boiling point and decrease the freezing point of certain products; which is the case of candies for example.

Sugars such as fructose have the ability to reduce water and microbiological activities as well as mold formation; making it for instance useless to refrigerate foods with high content of sugars, and provides an extensive shelf life. In baked products, sugars such as glucose, fructose, galactose, sucrose, lactose and maltose, play a role as substrate for fermentation (helps dough rising). Reducing sugars (e.g. monosaccharides) provide the brown coloring of products like some desserts or bread, thanks to the nonenzymatic browning reactions that

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control food quality, caramelization, Maillard and Strecker reactions. Finally, invert sugars2 play a textural role by producing a smoother product; e.g. candies (Davis, 1995; Sigman- Grant & Morita, 2003).

The role of fat. Fat plays essential functional properties in foods. By trapping the air during the creaming process in baked products, fat provides their structure. It is also responsible for the crisping character of fries or chips, by rapidly and uniformly transmitting the heat for example. Likewise, the chewiness and softness of foods are provided by their fat component melting points. Furthermore, the given fat content of a product determines its storage stability (Hahn, 1997). The moistness of cakes and the juiciness of hamburgers are determined by the water-holding quality of fats. Moreover, crispy and crunchy textures can be achieved by cooking in fats at temperatures above that of boiling water (Drewnowski, 1997b).

1.1.2. The organoleptic functions of salt, sugar and fat

Organoleptic3 functions refer to the properties of a food that are perceived by sense organs and are partially responsible for its palatability. Such properties include visual appearance, sound, smell, taste, texture, temperature, and trigeminal inputs of a food (Sørensen, Møller, Flint, Martens & Raben, 2003). During the present work, we are focusing on the orosensory qualities of foods. Taste qualities are known to be a primary driver of ingestion, especially in children (Birch, 1999; Drewnowski, 1997a). Although all sensory properties of a food, such as its appearance and/or smell might impact its intake (Drewnowski, 1997a; Rolls, Rowe & Rolls, 1982; Shepherd, 1988), the gustatory sensations from foods and beverages rank first among the drivers of an individual’s food choice (Glanz, Basil, Maibach, Goldberg & Snyder, 1998). Salt, sugar and fat for instance are known to enhance the palatability of foods, thanks to their flavoring properties, and their capacity to enhance other flavors within a food (Hegarty, 1995 in Lee, 2011). We will discuss in this section the taste, flavor and texture contribution of salt, sugar and fat in foods.

2 Invert sugars are defined by the Oxford dictionary as ‘a mixture of glucose and fructose obtained by the hydrolysis of sucrose’.

3 Organoleptic is defined by the Oxford dictionary as the ‘acting on, or involving the use of, the sense organs’.

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Salt (NaCl) is responsible for one of the five basic tastes, the salty taste (Chandrashekar, Hoon, Ryba & Zuker, 2006). Humans’ avidity for salty taste is not due to a ‘sodium appetite’

(a desire for sodium) as it is the case for animals, but is most probably related to a ‘salt appetite’ (seeking the taste of NaCl), an attraction to the taste of salt independently from the subject’s sodium status (Leshem, 2009). Salt is a flavor enhancer (Shepherd, 1988), as it reinforces the flavor of other ingredients present in a food, due to its “salting out” effect.

This effect is a result of ‘an increase in headspace concentration of aroma compounds presumably related to the reduction in available solvent in the liquid phase resulting from the presence of salt’ (Salles et al., 2011). In other respects, salt ‘selectively filter flavors’:

unpleasant ones -i.e. bitterness- are suppressed, while palatable ones -i.e. sweetness- are not, thereby ‘increasing the salience and/or intensity of the latter’ (Breslin & Beauchamp, 1997). Salt is also known to help controlling texture and consistence of certain preparations by interacting with other components (Doyle & Glass, 2010): in baked products an optimal amount of salt ensures loaves of bread with adequate texture; and in meat products, salt enables the binding between proteins and water thus enhancing tenderness.

Sugars, another of the five basic tastes, generally taste sweet (Chandrashekar et al., 2006). In the case of sweet, the color of the sample might influence its organoleptic judgment. Indeed, studies cited by Rose Marie Pangborn demonstrated that an unflavored solution with a red color will be judged as sweeter than the same but less red solution, and pear nectar with a green coloring will be judged as less sweet than the same nectar without coloring. In 1987, R. M. Pangborn described a salting-out mechanism by which sugars increase the concentration of volatile aroma compounds in the headspace (Pangborn, 1987).

In foods, sugars impart texture and provide the viscosity and the density of products such as in dairy products; they also responsible for other functions such as the crispiness and the brittleness of cookies for example (Davis, 1995).

Studies have shown that fat contributes to several organoleptic properties such as the aroma, flavor and texture of foods (Drewnowski, 1997b; Drewnowski, 2000). Fats carry, enhance and release the flavors of other food ingredients. Fat is a carrier of aroma compounds, most of which are fat-soluble and thus are associated with the lipid phase (Yackinous & Guinard, 2000). The first sensory impact of fat is the perception of fat-soluble

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aroma compounds, first through the nose -orthonasal- or through the mouth -retronasal- (Drewnowski, 1997b). In fact, reduction of fat negatively impacts aroma release, as fat affects the partition of volatile compounds between the food and the air phase in the mouth (Bayarri, Taylor & Hort, 2006). That explains the greater perception of fat in some products such as potato chips when the olfactory dimension was present, while wearing nose-clips (suppressing the olfactory dimension) lowered the fatty ratings (Yackinous & Guinard, 2000).

The second impact of fat is on texture, as it is a ‘critical part of the physical food matrix’

(Yackinous & Guinard, 2000). Fat contributes to many textural properties such as viscosity, mouth-coating, cohesiveness, crispiness and hardness, etc. (Mela, 1992). In dairy products, fats provide smoothness, thickness and viscosity; whereas the cooling feel of fats in the mouth is the characteristic feature of butter and cream (Drewnowski, 1997b). Another textural characteristic of importance in dairy products is their ‘creamy’ or ‘unctuous’

attribute. As described by Tournier and co-workers, when it concerns dairy products, French consumers use the term ‘crémeux’ the French for ‘creamy’ as a synonym of ‘unctuous’ the term widely used in non-French based studies. Moreover, ‘creaminess appears to be an integrated concept, which is related to textural properties, fattiness, flavour and even the pleasantness of food products’ (Tournier, Martin, Guichard, Issanchou & Sulmont-Rossé, 2007).

1.1.3. The nutritional and physiological functions of salt, sugar and fat

Salt. Sodium is a vital and essential nutrient for the body. Several studies cited by Durack and colleagues (2008) estimate that for an adult, average physiological requirements for salt do not exceed 4 g per day (1.6 g of sodium), and is often estimated around 1 or 2 g per day (AFSSA, 2002; Durack et al., 2008). The WHO estimates physiological needs of sodium to be around 10-20 mmol per day (230-460 mg of sodium or 0.575-1.15 g of salt); (Eliott & Brown, 2006). Children’s physiological needs for salt were not yet studied and thus need to be established (He & MacGregor, 2006).

Sodium maintains water balance in body cells and extracellular fluid volume. It is also essential for the transmission of nerve impulses, for muscle and nerve activities for instance.

It helps maintaining water homeostasis and constant biological parameters with regard to changes of external environment (Durack et al., 2008; Garcia-Bailo, Toguri, Eny & El-Sohemy,

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2009; Spetter, Smeets, de Graaf & Viergever, 2010). So, low salt intake is likely to cause muscle cramps, weakness and fatigue, and might have adverse effects on thermoregulation in high environmental temperatures for example. Extreme depletions can even be fatal (SACN, 2003). When dietary sodium exceeds physiological needs, plasma sodium level is maintained constant in the body thanks to the excretion in urine and sweat to a certain upper limit (Durack et al., 2008). As it will be discussed in section 1.3., due to the important role of salt in maintaining electrolyte balance, in regulating blood pressure and blood volume and in water homeostasis, its intake recommendations are more precise than those for sucrose.

Sugar. Glucose resulting from the digestion of sugars (mono- and disaccharides) is one of the energetic substrates for the body and for the brain. When it is not used, glucose is stored as glycogen in the liver and in the muscles; and if the body is lacking energy, the glucose is released -or remains- into the bloodstream to be delivered and metabolized into the brain, kidney, muscle cells and adipocytes (Sigman-Grant & Morita, 2003). Moreover, a strong physiological role of sweet solutions (glucose or sucrose) is observed in neonates. In fact, when a sweet solution is orally administered, it exerts a pain-relief effect; this effect is specifically attributed to the taste of sweet and not to its post-ingestive consequences (Nicklaus & Schwartz, 2008). This analgesic effect is observed when 1 ml of a 30% glucose solution is administered, and the effect was not seen to induce tolerance, even if administered three times a day for 3 to 5 days (Eriksson & Finnstrom, 2004).

Fat. Fat is present in the body as cell lipid droplets in adipose tissue and FAs are gathered in there and are stored as TGs. That makes fat the macronutrient providing the most concentrated source of energy to the body. For example, 55% of the energy that newborns get from breast milk comes from fat; that insures a rapid growth, as well as brain and nervous system development. When it concerns total FAs, physiological needs4 are equivalent to 30% of energy intake (EI) in healthy adults with an energy intake equivalent to

4 The physiological needs for lipids established by the report of the French ANSES are in accordance with international data.

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2000 kcal per day, whereas no precision in given for children (ANSES, 2011). Before going forwards, few definitions and distinctions must be made.

SFAs are synthesized by the human body (in the brain, liver and adipose tissue) and their physiological functions differ according to their type (ANSES, 2011). Butyric acid (C4:0) has a positive action in apoptosis of tumor cells. Medium-chain SFA such as caproic (C6:0), caprylic (C8:0) and capric (C10:0) acids, are a rapid source of energy and have a protective effect against obesity in humans, as they are rapidly absorbed and oxidized in the liver; they have an antiviral effect; and they also have no hypercholesterolemic effect and are not associated to CVD risk contrarily to long-chain SFAs. Indeed, long-chain SFAs such as lauric (C12:0), myristic (C14:0) and palmitic (C16:0) and stearic (C18:0) acids, are a great source of energy, and have functional roles in cell membranes. Although, some of these especially lauric, myristic and palmitic acids may have deleterious effects on health in case of excess, due to their atherogenic effects (ANSES, 2011).

Part of the MUFAs is synthetized by the body, and the other part is provided by the diet.

They also constitute cell membranes and are of importance for enzyme, transporter and receptor activities.

PUFA play a major role in cell walls, as they insure cell communication and hormone production. This family includes essential fatty acids (EFA) as they cannot be synthesized by the body. Those are the linoleic acid (LA, C18:2 n-6) the precursor of the n-6 or ω6 FA family, and the alpha linolenic acids (ALA, C18:3 n-3) the precursor of the n-3 or ω3 FA family. They are precursors for other fatty acids such as long chain-PUFAs: arachidonic (ARA, n-6), eicosapentaenoic (EPA, n-3) and docosahexaenoic (DHA, n-3) acids, so called ‘conditionally essentials’ or ‘non-essential FA’. Physiological needs for French healthy adults are equivalent to 2 (4.4 g/d), 0.8 (1.8 g/d) and 0.1% (250 mg/d) of EI respectively for LA, ALA and DHA (ANSES, 2011). Besides being essential for insuring the functions of the central nervous system, LA and ALA (and their metabolites) are also important in the early development of visual acuity and cognitive functions (Macé, Shahkhalili, Aprikian & Stan, 2006). These long- chain-PUFAs can be synthesized by humans and animals, providing that their precursors are delivered in sufficient quantities through the diet. Some FAs contribute to the structure of phospholipids (PL), the major constituents of all body cell membranes in particular in neural cells, as they modulate their fluidity and their activity. Other FAs contribute to the structure of sphingolipids, also present in cell membranes and responsible for cell recognition and

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signaling. PUFA are of great importance for hemostasis, platelet aggregation, immune reactions, cell differentiation, reproduction and also gene regulation (ANSES, 2011).

Fat is also important if not necessary to vehicle and facilitate the absorption of fat-soluble vitamins such as vitamin A, D, E and K (Reed, Mela & Friedman, 1992). Suboptimal fat intake might impart health problems such as the supply of minerals, fat-soluble vitamins and caloric insufficiency (Rogers & Emmett, 2001).

1.2. Public health concerns related to salt, sugar and fat intake

1.2.1. Diet-related health problems in relation to salt, sugar and fat intake

Scientific evidences highlight the link between diet quality and several chronic diseases.

Some of these diet-related diseases are obesity, diabetes, cardiovascular diseases, cancer, osteoporosis and dental diseases (WHO, 2003). In addition to the costly burden to health care services, these diet-related diseases represent a major public health preoccupation worldwide, as they were responsible for approximately 60% of the reported deaths in the world in 2001. Although deaths due to these diseases have, for a long time, been identified only in adults, they start to appear in childhood and represent a source of concern. Recent literature brings evidence that the diet during early childhood might predispose an individual to develop diet-related health problems in later adult life (Bateson et al., 2004). It may be possible to reverse this tendency by acting on diet improvement in order to prevent rather than heal. Several diet-related diseases were linked to the intake of some nutrients such as salt, sugar and fat, as reported below.

1.2.1.1. Salt

Although salt has for long been thought to be a health preservative (by killing/limiting food-borne pathogens), it is nowadays considered as a health threat in response to an excessive consumption (Doyle & Glass, 2010). Excess dietary salt intake was shown to be responsible for several health problems and is strongly presumed to influence the rise in blood pressure (BP) or hypertension with age (Simons-Morton & Obarzanek, 1997). BP subsequently pre-disposes individuals to CVD, a leading cause of death in developed

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countries (He & MacGregor, 2004; WHO, 2003), as BP is responsible for 62% of strokes and 49% of coronary heart diseases (He & MacGregor, 2010).

The most debated effect of salt on health is probably its effect on the early pathogenesis of hypertension. Neither the observational studies, nor the randomized experimental studies (of short- or long-term) reviewed by Geleijnse and Grobbee could establish a direct association between blood pressure and early sodium intake (Geleijnse & Grobbee, 2002).

Besides the biological plausibility exposed by the authors, they state that it is not clear to date if children’s hypertension “tracks” into adulthood. A more recent meta-analyses conducted by He and MacGregor, concluded that in order to prevent the rise of blood pressure in adulthood, a reduction in dietary salt intake during childhood would be beneficial (He & MacGregor, 2006). The results of this later meta-analysis are in accordance with earlier ones, in that higher sodium intake is related to higher BP in children and adolescents (Simons-Morton & Obarzanek, 1997). Thus, the importance of diet during childhood in the prevalence of later health concerns has to be taken into account. The inconsistency of the results obtained by different studies investigating the link between BP and salt intake in children or adolescents, could be due to several factors, such as the use of different methodologies to investigate dietary salt intake (reviewed in 1.4.), the adjustment or not for confounders such as total energy intake, physiological activity etc. (Geleijnse &

Grobbee, 2002), or due to the short term of the considered studies He & MacGregor, 2010.

Concerning the epidemiological approach, a large international study aiming at evaluating the link between BP and salt intake called INTERSALT study (1985-87), includes 52 communities of 10 079 adults aged 20-59 years, from 32 countries, with variable salt intakes (from 6 to 25 g/day), found an association between the rise in BP with age and salt intake (Intersalt Cooperative Research Group, 1988 cited by He & MacGregor, 2010); a high sodium intake during life is partially responsible for BP increase with age. Moreover, other epidemiological studies such as the INTERMAP and the Norfolk Cohort of the European Prospective Investigation into Cancer (EPIC-Norfolk) studies underline the importance of salt intake in determining the levels of population BP (Zhou et al., 2003 and Khaw et al., 2004 cited by He & MacGregor, 2010)

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The report of the AFSSA (France) draws the reader’s attention to the fact that literature data do not allow a generalization to the whole population of the potential harmful effect of salt intake for health especially hypertension (AFSSA, 2002). This observation is shared by other scientists, pointing the uncertainty about the value of low-salt diets for the management of hypertension (Alderman, Cohen & Madhavan, 1998). Besides, the effect of dietary sodium on blood pressure may only be detectable in populations in which the range of sodium intake is sufficiently large, or in population subgroups that have a specific sensitivity for the effects of sodium (Watt et Foy, 1982; Grobbee 1991 and Weiberger 2000 in Geleijinse et Grobbee, 2002). However, He and MacGregor maintain the necessity to reduce salt intake in the whole population in order to efficiently lower BP. This effect on BP would be more efficient if salt intake reduction is included in a global well balanced diet (rich in fruits, vegetable, low-fat dairy products) as it was proven by the DASH study (Dietary Approach to Stop Hypertension); He & MacGregor, 2010.

A review by Durack and colleagues, listed other illnesses caused by excessive salt intake, such as the development of kidney diseases as well as early kidney damages, and the aggravation of asthma conditions. Moreover, an increased intake of salt favors sodium and calcium excretion in urine, leading to a decrease in bone density and to the onset of osteoporosis (Durack et al., 2008). Salt and salt-preserved foods were also shown to be linked to the prevalence of certain cancers (e.g. colon, stomach or kidney cancers); WHO, 2003.

1.2.1.2. Sugar

It was widely advanced that the etiology of dental caries is linked to dietary sugars, a report by the WHO/FAO experts sets that “a low free sugars consumption by a population will translate into a low level of dental caries” WHO, 2003. However, a recent review conducted by Ruxton and colleagues, on publications available from 1995 to 2006, is not affirmative about a systematic relationship (Ruxton, Gardner & McNnulty, 2010). The 46 studies reviewed included experimental and epidemiological studies, found the relationship between sugar and caries to be either null, positive or complex (with significance observed only in some subgroups where tough brushing was infrequent for example). The reason of

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this inconsistency may be due to the use of invalidated tools to record intake, or to the lack of consideration in some studies of some confounders such as oral hygiene, intake of sugar per se or of sugar-rich foods, consideration of the level of oral bacteria, food oral clearance etc. (Ruxton et al., 2010); thus, highlighting the complexity of demonstrating and affirming such a simple causal relationship. However, the importance of lowering sugar intake and brushing teeth with fluoride in order to stop or at least delay the prevalence of dental caries remains valid (Reed & McDaniel, 2006). The report edited by the WHO/FAO experts also concluded that “evidence for a relationship between dental caries and both amount and frequency of free sugars was described as ‘convincing’” WHO, 2003.

In other respects, the link between sugar intake and the occurrence of some cancers (breast, colorectal or lung), or between sugar intake and metabolic syndrome5 is not yet fully established and conclusions vary from a study to another. Although the link between intake of sugars and attention-deficit hyperactivity disorders (ADHD) was suggested in children, all reviews of the subject conducted between 1995 and 2003 failed to bring any scientific proof (Ruxton et al., 2010). However, the link between high carbohydrate, high sweet food intake and mood is more likely; for instance depressed persons prefer this kind of foods (Christensen and Somers, 1996 cited by Ruxton et al., 2010). A similar positive effect of sugar on mood was described by other authors (Reed & McDaniel, 2006); some even considered carbohydrate snacks as ‘self-medications’ due to their positive effects to improve mood state, relieve depression and fatigue (Lieberman, Wurtman & Chew, 1986).

1.2.1.3. Fat

In the case of fat, both an excessive and a poor intake are linked to health problems in humans. On the one hand, excess dietary intake of fats was shown to be strongly influencing the risk of cardiovascular diseases, as it affects blood lipids, blood pressure and arterial functions among other things (WHO, 2003). The PNNS group in France is in charge of

5 The metabolic syndrome consists of a cluster of disease states, including 3 of the following 5 criterion: central obesity, hypertriglyceridemia, low levels of high-density lipoproteins (HDL), elevated BP, impaired glucose tolerance; ANSES, 2011.

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evaluating and advising for lipid use. It stated that health problems due to fat might be caused by the excess of fatty acid intake in relation to needs (PNNS, 2009); keeping in mind their qualitative effects. A recent review by Brown and his colleagues goes around that issue and provides an overview of the impact of fats on some diseases such as the metabolic syndrome and the importance of the diet’s fat profiles on health (Brown et al. -chapter 21- in Montmayeur & Le Coutre, 2010). Moreover, the intake of saturated fatty acids in particular was linked to the increased concentration of cholesterol, a factor known to be linked to the prevalence of heart diseases (Montmayeur & Le Coutre, 2010). Thus, restricting the intake of SFAs, such as those found in dairy products or butter, appears of importance for ensuring cardiovascular health. On the other hand, a poor intake of PUFA (especially long-chain n-3) was linked to psychopathological and cognitive disorders such as depression, schizophrenia, ADHA and autism (ANSES, 2011).

1.2.2. Body weight and nutrient intakes

1.2.2.1. Definition of overweight and obesity

Overweight and obesity are defined by the WHO as an “abnormal or excessive fat accumulation that may impair health”. Obesity was recognized as a disease in 1997 by the WHO. The prevalence of overweight and obesity has become a threat for all public health services worldwide (World Health Organisation, 2000).

Overweight and obesity can be assessed objectively by using a universal index named Body Mass Index (BMI) or Quetelet index (Thibault & Rolland-Cachera, 2003). Researchers, clinicians and health professionals, defined this index using the subject’s weight (in kilograms) and height (in meters): BMI (kg/m²) = weight / height². It is a useful proxy measure of adiposity (Cole, Faith, Pietrobelli & Heo, 2005). Even if it does not measure body fat directly, it correlates to other direct measures such as underwater weighing and dual x-ray absorptiometry (DXA). This measure has the advantage for being inexpensive and easy to perform.

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1.2.2.2. Cut-offs and prevalence of overweight and obesity in adults

The WHO defines overweight as a BMI greater than or equal to 25 kg/m² and lower than 29.9 Kg/m², and obesity as a BMI greater than or equal to 30 kg/m² respectively (World Health Organisation, 2011).

In 2008, one in ten of the world’s adult population was obese and in 2010, overweight and obesity were responsible for more deaths around the world than do underweight (World Health Organisation, 2011). In France as in other countries, the prevalence of obesity increased in adult populations, as it evolved from 8.5% in 1997 to 14.5% in 2009 (ObEpi- Roche, 2009). The French INCA2 study conducted between 2006 and 2007, identified 36 % and 50 % of women and men, to be overweight or obese (AFSSA, 2009).

1.2.2.3. Cut-offs and prevalence of overweight and obesity in children

Due to the variations of body composition during growth, children and adolescents’ BMI is age and sex specific (Cole, 1990). Therefore, another measure of adiposity is the standard deviation (or z-score6) of BMI, calculated using the LMS method (Cole, 1990). It is “the deviation of the value for an individual from the mean value of the reference population divided by the standard deviation of the reference population”.

BMI-for-age curves were developed by several countries, with their own population references (Rolland-Cachera & Péneau, 2011). The French reference curves, established in 1982 and revised in 1991, use data from a sample of French subjects who participated to the International Growth Study conducted by the International Children’s Center, from 1953 to 1955 (Rolland-Cachera, Cole, Sempe, Tichet, Rossignol & Charraud, 1991; Rolland-Cachera, Sempé, Guilloud-Bataille, Patois, Péquignot-Guggenbuhl & Fautrad, 1982). In order to define overweight and obesity the thresholds defined for the French reference population are used along with those established by the International Obesity Task Force (IOTF) (Cole, Bellizzi, Flegal & Dietz, 2000; Thibault & Rolland-Cachera, 2003); these new curves, as depicted in figure 1, established under the PNNS program, are included in individuals’ health book.

6 http://www.cdc.gov/growthcharts/growthchart_faq.htm. Last access August 4th, 2011.

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In order to define overweight and obesity, cut-offs during childhood differ according to the source and thus to the reference data used. The IOTF references provide cut-off values based on percentiles passing through BMI 25 (IOTF-25 in the curve) and 30 kg/m² (IOTF-30 in the curve) at age 18, defining overweight and obesity respectively. Concerning French references they use all ranges from the 3rd to the 97th percentile. overweight is defined as a BMI >97th percentile, with two levels of obesity: level 1 when the value is between the 97th percentile of the French references and the IOTF-30, and level 2 when the value is above the IOTF-30 value as shown in Figure 1 (Thibault & Rolland-Cachera, 2003). Besides, the Center for Disease Control (CDC), defines children and adolescents as overweight when their BMI is greater than the 85th but lower than the 95th percentile; whereas pediatric obesity is defined as a BMI above the 95th percentile (Yanovski, 2001). These various references and growth parameters used by scientists across the literature, made it difficult to compare data from different studies and/or different countries, and to reach comparable conclusions on the prevalence of children’s overweight and obesity (Rolland-Cachera & Péneau, 2011; Salanave, Péneau, Rolland-Cachera, Hercberg & Castetbon, 2009).

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Figure 1. French Body Mass Index curve.

Body Mass Index curves for Girls adapted for the PNNS7 (Thibault & Rolland-Cachera, 2003), with cut offs and terminologies (Rolland-Cachera et al., 2002).

7 http://www.inpes.sante.fr/CFESBases/catalogue/pdf/IMC/courbes_enfants.pdf. Access date August 2011.

Overweight

Underweight

Body Mass Index

Age (years)

BMI curves for girls (0 to 18 years)

French references and International Obesity Task Force (IOTF) cut offs

Overweight

Underweight

Body Mass Index

Age (years)

BMI curves for girls (0 to 18 years)

French references and International Obesity Task Force (IOTF) cut offs

Level +2 France: … IOTF ≥ C-30 WHO ≥ +2 SD CDC ≥ 95th percentile

Level +1

France ≥ 97th percentile IOTF ≥ C-25

WHO ≥ +1 SD CDC ≥ 85th percentile

Level -1

France < 3rd percentile IOTF < C-17

WHO < -2 SD CDC < 5th percentile Overweight including obesity (WHO / IOTF)

Overweight

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During the work conducted in this thesis, the French reference data for children were used to calculate z-BMI, and international cut-offs for adults were used in studies implicating adults.

A persistent obesity at 6-8 years old is likely to track until adolescence and adulthood.

The WHO identified 43 million children under five to be overweight (World Health Organisation, 2000). In France, before the 90s, no national data on the prevalence of overweight and obesity were available. The only available data were conducted at the regional level, and the definition of obesity was based on the French references established in 1960 and published by Roland-Cachera and co-workers. A collective expertise conducted by Inserm (France), highlighted the fact that the prevalence of obesity (>97th percentile) in 5 to 12 year-old children, is equal to 3 % in 1960, rose in a 15 year period from 6 % in 1980 to reach 10-12 % in 1996 (Expertise collective Inserm, 2000; Rolland-Cachera et al., 1991). Since then, health authorities in France recognized the necessity to monitor children’s weight, and conducted several studies in order to follow its evolution. Thus, overweight concerns 10.9 to 14.3 % of the pediatric population and obesity 2.4 to 3.8 % as shown on Table 2.

Table 2. Evolution of the prevalence of overweight and obesity in French children from 1998 to 2007.

Year Population

(n; age) Overweight (%) Obesity (%) Ref.

INCA 1 1998-1999 1016 ; 3-14 years 11.7 3.5 [1]

National Study ECOG

protocol

2000 1582 ; 7-9 years 14.3 3.8 [2]

ObÉpi 2000 6084 ; 2-17 years 10.9 2.4 [3]

INCA 2 2006-2007 1146 ; 3-17 years 11.2 2.8 [4]

Cut-off references were those of the IOTF definition from Cole et al., 2000.

[1] Lioret, Maire, Volatier & Charles, 2007; [2] Rolland-Cachera et al., 2002; [3] Charles, Eschwege & Basdevant, 2008; [4] AFSSA, 2009. Adapted from the AFSSA report: AFSSA, 2009.

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